Trait‐independent habitat associations explain low co‐occurrence in native and exotic birds on a tropical volcanic island

Abstract On oceanic islands, strong human impacts on habitats, combined with introductions of exotic species, modify the composition of terrestrial bird assemblages and threaten their ecological functions. In La Réunion, an oceanic island located in the Madagascan region, a national park was established in 2007 to counter the ecosystem‐level effects of three centuries of habitat conversion, native species destruction and exotic species introductions. Here, we investigated how bird assemblages were structured in these human‐modified landscapes, 10 years before the national park set out its first conservation measures. We used a combination of multivariate statistics and generalized additive models to describe variations in the taxonomic and functional composition and diversity of 372 local bird assemblages, encompassing 20 species, along gradients of habitat composition and configuration. We found that native species were tied to native habitats while exotic species were associated with urban areas and man‐modified landscape mosaics, with some overlap at mid‐elevations. Species' trophic preferences were segregated along habitat gradients, but ecological traits had an overall weak role in explaining the composition of species assemblages. Hence, at the time of the survey, native and exotic species in La Réunion formed two spatially distinct species assemblages with contrasting ecological trait suites that benefited from antagonistic habitat compositions and dynamics. We conclude that our results support the analysis of historical data sets to establish reference points to monitor human impacts on insular ecosystems.


| INTRODUC TI ON
The Madagascan region is the smallest and the second most distinctive of the world's 11 zoogeographic regions (Holt et al., 2013).
Formed exclusively of oceanic islands spread throughout the western Indian Ocean, it is relatively species-poor but displays disproportionately high endemism rates. For instance, 41% of the region's 382 native terrestrial bird species are regional endemics. This percentage even rises to 75% in La Réunion, the second largest island of the region after Madagascar and the largest of the Mascarenes archipelago (Safford et al., 2015). However, assessments of human impacts on insular ecosystems are deficient in the Madagascan region, even on the best-studied islands such as La Réunion, hampering the establishment and evaluation of initiatives for the conservation of insular biodiversity.
On oceanic islands, long-term isolation favoured the evolution of ecosystems involving a low number of endemic species which support nonsubstitutable ecological functions, notably in birds (Boyer & Jetz, 2014;Kaiser-Bunbury et al., 2010;Şekercioğlu et al., 2016).
Birds' contributions to insular ecosystems have been particularly well investigated in islands of the Indo-Pacific, such as Hawaii (Barton et al., 2021) or New Zealand (Anderson et al., 2021). Plant-bird interactions likely to support key ecological functions are also documented in the Madagascan region, although case studies remain local and scarce. For instance, in La Réunion, the pollination of the endemic orchid Angraecum bracteosum by the endemic Reunion olive White-eye Zosterops olivaceus recalls the pollination of Clermontia (Lobelioideae: Campanulaceae) by endemic Hawaiian birds (Aslan et al., 2014;Micheneau et al., 2008). However, the extent to which these specialized plant-bird interactions still sustain their ecosystem functions in spite of the human-driven depletion of Madagascan avifaunas remains unknown (Albert et al., 2020;Anderson et al., 2021;Schleuning et al., 2014;Şekercioğlu et al., 2016).
The Madagascan region is sadly famous for its high extinction rates, especially in large frugivorous birds (Heinen et al., 2018). In La Réunion, the first human colonization occurred in the late 17th century, far later than in many other tropical archipelagos. It was accompanied by novel and intense pressures, which led many terrestrial bird species to severe range reductions or extinction. Since then, approximately two-thirds of the island's native vegetation has been converted for agriculture or replaced by exotic vegetation (Lagabrielle et al., 2009;Mourer-Chauvire et al., 1999). Rapid habitat destructions, on top of overhunting and other pressures, were likely the most critical cause for the extinction of all large vertebrates (Albert, Flores, Baider, et al., 2021), inducing ecosystem-level cascading effects in a few decades or centuries (Mourer-Chauvire et al., 1999;Strasberg et al., 2005;Whittaker & Fernández-Palacios, 2007). In particular, many of the common fleshy-fruited tree species on which frugivorous birds fed declined as lowland native forests were nearly eradicated (Albert et al., 2018). In turn, the extinction of frugivores, which sustained seed dispersal, amplified the decline of most fleshy-fruit plant species in the 300 years after the first European settlement (Albert et al., 2020;Albert, Flores, Baider, et al., 2021).
Conversely, the abundance and diversity of exotic plant species now peaks close to the middle of the elevation gradient (Tassin & Riviere, 2003), and wide extents of high-altitude landscapes have been converted into pastures (Strasberg et al., 2005).
Island endemic birds are characterized by low dispersal abilities, failure to cope with the lack of native food resources in human modified habitats, and high mortality rates due to introduced mammalian predators such as cats or rats. Conversely, exotic species that establish feral populations on islands unsurprisingly exhibit ecological traits associated with ecological opportunism, use of human resources and ability to colonize novel environments (Blackburn et al., 2009;Cassey, 2002;Duncan et al., 2003). Accordingly, the propensity of exotic bird species to invade islands from their initial introduction locations depends on an interaction between the invasibility of nonconverted native habitats and species' propensity for colonization, determined by their ecological traits and the conditions of their introduction (Alpert et al., 2000;Blackburn et al., 2009). The introduction of exotic species has in some instances compensated, or even exceeded in number, the man-mediated extinction of native and endemic species (Sax et al., 2002;Whittaker et al., 2014). However, native and exotic bird species exhibit low functional redundancy, and are segregated among habitats along elevational and anthropogenic disturbance gradients (Barnagaud et al., 2014(Barnagaud et al., , 2022Fischer & Lindenmayer, 2007;Whittaker & Fernández-Palacios, 2007).
Because of their trait and habitat differences, exotic species do not usually replace native species' lost ecological functions (Anderson et al., 2021;Duncan et al., 2003;Vila et al., 2011), except in idiosyncratic situations such as the replacement of Clermontia's native pollinators by introduced Zosterops in Hawaii (Aslan et al., 2014, but see Pejchar, 2015 for a contrasting example on seed dispersal also in Hawaii). Hence, although bird introductions increase taxonomic diversity (the diversity of species) and functional diversity (the diversity of ecological traits) at the island scale (Whittaker et al., 2014), their effect on the composition of local species assemblages and ecosystem functions remains unclear. For instance, among the 20 exotic bird species established in La Réunion since the 19th century, the Red-whiskered Bulbul (Pycnonotus jocosus) is the only one known to enter native forests, thus liable to modify the composition of native plant assemblages through the endozoochorous dispersal of exotic plants (Clergeau & Mandon-Dalger, 2001;Mandon-Dalger et al., 1999). Although these novel mutualistic interactions are identified, the extent to which they may favour plant invasions and ultimately trigger long-term changes in the composition of plant communities remains unknown.
Unlike many oceanic islands with comparable sizes, the land use patterns in La Réunion partly disentangle the distribution of native and converted habitats from altitudinal variation, offering the possibility to distinguish their respective influences on the distribution, composition and diversity of species assemblages (Plate 1).
Depending on the scale at which species respond to their environment and resources, the island's fine-grained mosaics of manmodified and native vegetation may either inflate contrasts in the functional composition of species assemblages within local habitats, or trigger biotic homogenization at the landscape scale (Byamungu et al., 2021;Cadotte et al., 2011;Diaz & Cabido, 2001;McGill et al., 2006). These features, concentrated on a relatively small study region, make La Réunion a particularly favourable study area to investigate the determinants of spatial variations in the composition of local bird assemblages. In particular, the weak correlation between altitude and human impact, at least up to the upper third of the elevation gradient, allows separating their respective roles on the cooccurrence or separation of exotic and native bird species among local assemblages.
Building on this specificity, we investigated spatial patterns

| Study location
La Réunion Island is a 3-million-year-old volcanic island, part of the Mascarene archipelago (Western Indian Ocean, 55°30' E and 21°05' S, Figure 1). Administratively, it is a french 'département d'Outre-Mer', which warrants the feasibility of long-term studies with the support of well-established local research institution and conservation stakeholders, a relatively rare feature in the Madagascan region. In the centre of the island, a plateau (Plaine des Cafres, ca. 1500 m above sea level) is flanked by two volcanoes (Piton de la Fournaise, 2631 m, active, and Piton des Neiges, 3069 m, extinct), descending into the coastal plain with an elevation change of 2000 m in 10-30 km. This topography causes a steep climatic gradient, with an average minimum ground temperature below 0°C above 1500 m in August, above 1800 m from June to October, and above 2300 m all year round.
At the highest point, the annual temperature variation ranges from −10°C to +26°C (Cadet, 1974;Raunet, 1991). The study area, located on the leeward side of the island, has a slope of about 0.15 m per m and an annual rainfall ranging from 500 mm at sea level to 2000 mm on the highest mountain slopes (Raunet, 1991). The vegetation is organized in elevational belts arranged from sea level to mountain tops. Partly orthogonal to this habitat gradient is a gradient of human habitat conversion. The original ecosystems have been modified earlier and more intensively at low elevations; patches of native tropical mountain forests still remain at mid elevations (NATI in Table 1, the P L AT E 1 The diversity and spatial structure of habitats in La Réunion island. (a) Background: exotic savannas, and sugar cane crops at low elevation, middle ground: mosaics of exotic thickets, woodlands along cliffs, foreground: mid-evelation mosaics of pastures and fallows. Suburban and urban habitats are present at all elevation levels. (b) Background: slopes of the Piton des Neiges massif (3070 m asl) covered with high elevation ericoid thickets, mid-ground: pastures in the central mid-elevation plain and mosaic of exotic plantations and native forests on higher ancient craters, foreground: native ericoid thickets on the lower slopes of the Piton de la Fournaise massif (2646 m asl). (c) View of a steep high cliff in the centre of the island with native forest of variable stature depending on local slope. All photographic credits (c) Jean-Yves Barnagaud. most important remaining native forest type in terms of surface and conservation). High elevations are still mostly uninvaded and covered by endemic vegetation (HIER and ACFO in Table 1, Albert, Flores, Ah-Peng, Cadet, 1980). The main habitat belts sampled in this study can roughly be categorized into coastal urbanized plains (0-50 m), savannah (50-300 m), sugarcane monoculture TA B L E 1 Habitat types used in the study and acronyms.

F I G U R E 1
Location of La Réunion island (a) and sampling design (b). The 38 red crosses depict points removed from the analysis due to missing data. Background layer: elevation raster (Jarvis et al., 2008).
(300-800 m), rural landscapes with crops (800-1200 m), primary forest mixed with pastures and planted forests (1200-1800 m), heathlands dominated by ericaceous plants (1800-2600 m) and bare soils with sparse herbaceous vegetation (2600-3069 m). and dry areas such as depressions, ridges and mires were avoided, as well as places too close to feeding troughs in grasslands, because they attract granivorous species.

| Habitat data
Landscape composition within a 150 m radius around each point count was characterized as the proportion of the total surface covered by 15 habitat categories (Table 1)

| Species' status and ecological traits
From the 23 species recorded at least once on the point counts, we discarded three species observed less than three times, since we considered them to be insufficiently represented to assess their habitat affinities (these species are listed in Appendix S1).
We defined species' status based on Safford et al. (2015) as ei-

| Statistical analyses
We summarized the variation of these five traits among the 20 species in a Hill & Smith analysis (an ordination method for tables mixing quantitative and qualitative variables, Hill & Smith, 1976) in order to explore the ecological overlaps and separations between native and exotic species. We then explored trait-habitat associations for the 20 species and 372 points in a three-table ordination method known as the RLQ analysis (Doledec et al., 1996), which links a matrix of environmental variation across sampling sites ( We visually explored the RLQ space to search for trait-habitat associations that may distinguish native from exotic species, and tested the robustness of trait-habitat associations through two complementary permutation models (Thioulouse et al., 2018, p. 231). The  Table 1. Background layer: elevation raster (Jarvis et al., 2008). neighbourhood was so low (Moran's I < 0.05 within a few kilometers) that we did not proceed with further correction.

| Trait overlap between native and exotic species
The two first axes of the Hill & Smith analysis summarized 23 and 16% of the total trait variation among the 20 species (third axis 14%, disregarded). The 20 species were evenly dispersed in the multivariate trait space, indicating relatively low ecological redundancy and few extreme strategies with respect to the traits used ( Figure 3).

| Native and exotic species' distributions along the elevation and habitat gradients
Native and exotic species were intertwined along the elevation gradient, but natives tended to predominate at higher altitudes and were virtually absent from coastal sites dominated by exotics Native species tended to avoid the most human-disturbed and fragmented habitats (higher counts in the negative side of PC2,

F I G U R E 3
The ecological trait space of 22 bird species based on five ecological traits (biogeographic origin, main diet, dietary specialization, foraging vegetation strata and log-transformed body mass), with convex hulls separating native (N) and exotic (E) species. Species' acronyms are defined in Appendix S1.

| Diversity-environment associations
The GAMs showed that species richness, Shannon's index and functional dispersion varied non-linearly along PC1 ( Figure 6) and to a lesser extent along PC2 (Figure 7). Species richness and Shannon's index exhibited hump-shaped relationships with PC1, with a maximum slightly shifted towards low-elevation areas (Figure 6a,d, positive scores), mainly due to the near-absence of native species in coastal plains ( Figure 6b). Inversely, exotic species richness and Shannon's index decreased steadily from lower to higher elevations (Figure 6c,f, i.e. increased along PC1). Total and exotic species' functional dispersion decreased slightly from lower to higher elevations (Figure 6g,i), but peaked at mid-elevations for native species (Figure 6h). F I G U R E 5 Trait-environment associations in a RLQ space (projection of habitat variables in (a), traits in (b), with exotic and native species' convex hulls). See acronyms for habitat types in Table 1.
Total species richness was depleted, and Shannon's index was slightly lower, in homogeneous sites with either native or exotic habitats (negative PC2 values, Figure 7a Inversely, the highest native species richness and diversity occurred in homogeneous native habitats, then declined slightly to a lower plateau with high variation (Figure 7b,e). FDis varied little along PC2 overall (Figure 7g). However, native species' FDis was slightly higher in homogeneous sites with native habitats (negative PC2 values in Figure 7h). Conversely, it increased slowly towards urban areas and exotic thickets up to a plateau for exotic species (positive PC2 values in Figure 7i).

| DISCUSS ION
Most native species were tied to mid-and high-altitude habitats dominated by indigenous vegetation, while the abundance distributions Converging with this niche-based interpretation, native and exotic species showed distinct ecological trait syndromes and were well separated in the RLQ space. We did not detect any phylogenetic signal contributing to shape these trait-environment relationships, which may be due to lack of statistical power, but more likely suggests that native and exotic species' distributions along the island environmental gradients do not stem from niche conservatism alone. This pattern aligns with results obtained in New Zealand, where exotic and native species also bear distinct trait syndromes and habitat preferences at a landscape scale (Barnagaud et al., 2022). In the case of La Réunion, traitenvironment relationships were predominantly explained by the distribution of species along environmental gradients rather by than traits themselves, suggesting that habitat barriers are independent from the traits we considered.
Still, we found that most frugivorous, insectivorous and nectarivorous native species were associated with high elevation and native forests, and did not come in contact with ground-dwelling omnivorous and granivorous exotic species, which are limited to man-modified habitats. Irrespective to whether or not ecological traits trigger an ecological filter, these results conform to the hypothesis that exotic species opportunistically remained confined to their historical habitats of introduction (Blackburn et al., 2013;Duncan et al., 2003), even though successfully introduced species usually exhibit traits enabling them to cope with novel environments (Blackburn et al., 2009). Conversely, native species may not be excluded from modified landscapes because their ecological traits prevent them from using man-related resources, but more likely due to other processes such as predation, competitive exclusion by exotic species, fine-grained ecological specialization, or preference for large extents of undisturbed habitats (Parlato et al., 2015).
Native aerial feeders such as Reunion Harrier, Mascarene Swiflet and Mascarene Martin had wider abundance distributions along the axis of habitat heterogeneity and were closer to exotic species than other native species in the RLQ space. These species cover large distances for foraging and thus depend less on the composition of local habitats where they were detected. Conversely, the frugivorous Red-Whiskered Bulbul was closer to native forest species than most other exotic species in the RLQ space. This recently-introduced bulbul is currently restricted to ecotone areas and infrequently enters native forests, but it has a high propensity to fast colonization after introduction and naturalization (Clergeau & Mandon-Dalger, 2001), enabling it to rapidly adapt to novel environments (Amiot et al., 2007). It is also well known for spreading invasive exotic plant species through zoochory (Mandon-Dalger et al., 1999).
for native plant assemblages, which can moreover be affected by a reduction of their dispersal by local functional extinctions of native birds (Anderson et al., 2021).
Diversity patterns were in line with species-level analyses. Native species reveal hump-shaped curves of diversity along the mixed elevation/habitat type gradient (PC1), reflecting the higher availability of native habitats at mid-elevations. Meanwhile, monotonous variation in all forms of exotic species' diversity was coherent with their reluctance to enter native habitats and generally to disperse out of human settlements (Duncan et al., 2003;Sol et al., 2017).
Interestingly, the role of habitat heterogeneity (PC2) was low for native species, although they were more diverse in non-fragmented native habitats. By contrast, and as expected, exotic species were clearly more diverse in habitat mosaics, corresponding to former forest areas converted to agriculture and urban settlements. Functional dispersion also matched these patterns, suggesting that traits are sampled in local assemblages according to species richness rather than under the influence of strong ecological filters, in coherence with the permutation tests performed on the RLQ analysis.

| CON CLUS ION
As on other islands, the avifauna of La Réunion is not a single 'novel' species assemblage (Lugo et al., 2012), but consists of two distinct species assemblages separated by local habitat, which merge together at the landscape scale mostly around mid-elevations where sufficient amounts of native habitats persist within an otherwise man-modified matrix. Apart from the specific case of the Redwhiskered Bulbul, which could still be undergoing a positive colonization dynamic, recent field observations did not suggest substantial changes in this segregation pattern. However, La Réunion habitats and landscapes have changed in the 25 years since our data collection, due to the conflicting effects of increasing anthropogenic pressures and efforts to preserve wide expands of native habitats in the National Park. Replicating our field protocol may allow a quantitative, landscape-level overview of the consequences of these changes for the composition of bird assemblages. Given the high pace of ecosystem-level changes experienced on oceanic islands and its consequences for endemic insular biodiversity, we suggest that long-term studies and surveys become a priority for local conservationists and stakeholders. We also advocate in favor of further analysis of historical data sets on other islands, including still unpublished data wherever they exist, to increase the availability of reference points enabling the evaluation of conservation-oriented policies in protected areas, especially when established on insular ecosystems.

CO N FLI C T O F I NTER E S T S TATEM ENT
The authors declare no competing interests.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data and R scripts related to this study are archived on